Inference of interactions in cyanobacterial–heterotrophic co-cultures via transcriptome sequencing

Abstract

We used deep sequencing technology to identify transcriptional adaptation of the euryhaline unicellular cyanobacterium Synechococcus sp. PCC 7002 and the marine facultative aerobe Shewanella putrefaciens W3-18-1 to growth in a co-culture and infer the effect of carbon flux distributions on photoautotroph-heterotroph interactions. The overall transcriptome response of both organisms to co-cultivation was shaped by their respective physiologies and growth constraints. Carbon limitation resulted in the expansion of metabolic capacities, which was manifested through the transcriptional upregulation of transport and catabolic pathways. Although growth coupling occurred via lactate oxidation or secretion of photosynthetically fixed carbon, there was evidence of specific metabolic interactions between the two organisms. These hypothesized interactions were inferred from the excretion of specific amino acids (for example, alanine and methionine) by the cyanobacterium, which correlated with the downregulation of the corresponding biosynthetic machinery in Shewanella W3-18-1. In addition, the broad and consistent decrease of mRNA levels for many Fe-regulated Synechococcus 7002 genes during co-cultivation may indicate increased Fe availability as well as more facile and energy-efficient mechanisms for Fe acquisition by the cyanobacterium. Furthermore, evidence pointed at potentially novel interactions between oxygenic photoautotrophs and heterotrophs related to the oxidative stress response as transcriptional patterns suggested that Synechococcus 7002 rather than Shewanella W3-18-1 provided scavenging functions for reactive oxygen species under co-culture conditions. This study provides an initial insight into the complexity of photoautotrophic-heterotrophic interactions and brings new perspectives of their role in the robustness and stability of the association.

Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals

“…Peptidoglycan and lipopolysaccharides are components of the bacterial cell wall and outer membrane, and both have been suggested to mediate cell-cell recognition and signaling (Dworkin, 2014). Similar changes have been observed in different Synechococcus strains in response to co-culture (Tai et al, 2009;Beliaev et al, 2014). In response to nutrient starvation, the expression of these genes either did not change, or they were less abundantly expressed (Tolonen et al, 2006;Martiny et al, 2006;Thompson et al, 2011).…”

“…Whether this is in response to specific metabolic exchange, to changes in the oxidative levels of the cell or to general cell stress is currently unclear. Third, both Prochlorococcus strains are likely responding specifically to the presence of other cells in co-culture, through modification of the cell wall and membrane (a common occurrence in co-culture; Tai et al, 2009;Beliaev et al, 2014) and, in the case of MIT9313, increased expression of genes potentially involved in the production of or response to antimicrobial or signaling compounds (infochemicals). These include transporters and the prochlorosin and CCRG-2 gene families.…”

Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

“…Indeed, transcriptional analysis of a SynechococcusShewanella co-culture found that 14% of the changes in the Synechococcus transcriptome were affiliated with transport processes (Beliaev et al, 2014). Similarly, after 1 day of co-culture the relative transcript abundance of components for at two ABCtype transporters (PMN2A_1780 and PMN2A_1891) increased in Prochlorococcus, whereas another, PMN2A_1455, decreased.…”

“…Interactions between autotrophs and heterotrophs are central to the marine food web, as heterotrophic bacteria are dependent on photosynthetically fixed organic carbon supplied by primary producers. Autotrophheterotroph interactions have been shown to impact the autotroph as well, as work in the cyanobacterium Synechococcus has shown that co-culture impacts many cellular processes including carbon metabolism and stress responses (Tai et al, 2009;Beliaev et al, 2014). Growth of Prochlorococcus-the numerically dominant phytoplankter in the world's oceans (Flombaum et al, 2013)-in culture is improved by the presence of certain heterotrophs in terms of longevity, stationary phase cell density and ability to grow from low cell density (Sher et al, 2011).…”

Transcriptomic Responses of the Interactions between Clostridium cellulovorans 743B and Rhodopseudomonas palustris CGA009 in a Cellulose-Grown Coculture for Enhanced Hydrogen Production

“…Beliaev et al have analyzed the photoautotroph-heterotroph interactions between a cyanobacterium and a marine facultative aerobe with transcriptome sequencing. Their results have not only provided insights into the interactions between cyanobacteria and heterotrophs but also allowed the formulation of new hypotheses on cyanobacterial-heterotrophic interactions (24). Furthermore, Men et al have characterized the interactions of a dechlorinating coculture and triculture by transcriptome and proteome analyses.…”